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Article

Impacts of Elevated Atmospheric CO2 and N Fertilization on N2O Emissions and Dynamics of Associated Soil Labile C Components and Mineral N in a Maize Field in the North China Plain

by
Fen Ma
1,
Ming Li
1,
Na Wei
1,
Libing Dong
1,2,
Xinyue Zhang
1,
Xue Han
1,
Kuo Li
1 and
Liping Guo
1,*
1
Key Lab for Agro-Environment, Ministry of Agriculture and Rural Affairs, Institute of Environment and Sustainable Development in Agriculture, Chinese Academy of Agricultural Sciences, Beijing 100081, China
2
College of Agriculture, Shanxi Agricultural University, Jinzhong 030801, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(2), 432; https://doi.org/10.3390/agronomy12020432
Submission received: 6 December 2021 / Revised: 21 January 2022 / Accepted: 5 February 2022 / Published: 9 February 2022
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Abstract

:
The elevated atmospheric CO2 concentration (eCO2) is expected to increase the labile C input to the soil, which may stimulate microbial activity and soil N2O emissions derived from nitrification and denitrification. However, few studies studied the effect of eCO2 on N2O emissions from maize field under the free-air CO2 enrichment (FACE) conditions in the warm temperate zone. Here, we report a study conducted during the 12th summer maize season under long-term eCO2, aiming to investigate the effect of eCO2 on N2O emissions. Moreover, we tested zero and conventional N fertilization treatments, with maize being grown under either eCO2 or ambient CO2 (aCO2). We hypothesized that N2O emissions would be increased under eCO2 due to changes in soil labile C and mineral N derived from C-deposition, and that the increase would be larger when eCO2 was combined with conventional N fertilization. We also measured the activities of some soil extracellular enzymes, which could reflect soil C status. The results showed that, under eCO2, seasonal N2O and CO2 emissions increased by 12.4–15.6% (p < 0.1) and 13.8–18.5% (p < 0.05), respectively. N fertilization significantly increased the seasonal emissions of N2O and CO2 by 33.1–36.9% and 17.1–21.8%, respectively. Furthermore, the combination of eCO2 and N fertilization increased the intensity of soil N2O and CO2 emissions. The marginal significant increase in N2O emissions under eCO2 was mostly due to the lower soil water regime after fertilization in the study year. Dissolved organic C (DOC) and microbial biomass C (MBC) concentration showed a significant increase at most major stages, particularly at the tasseling stage during the summer maize growth period under eCO2. In contrast, soil mineral N showed a significant decrease under eCO2 particularly in the rhizospheric soils. The activities of C-related soil extracellular enzymes were significantly higher under eCO2, particularly at the tasseling stage, which coincided with concurrent increased DOC and MBC under eCO2. We conclude that eCO2 increases N2O emissions, and causes a higher increase when combined with N fertilization, but the increase extent of N2O emissions was influenced by environmental factors, especially by soil water, to a great extent. We highlighted the urgent need to monitor long-term N2O emissions and N2O production pathways in various hydrothermal regimes under eCO2.

1. Introduction

With the extensive combustion of fossil fuel and other anthropogenic activities since the industrial revolution, the atmospheric CO2 concentration has increased to 413.2 ppm in 2020 [1], and is predicted to reach 550 ppm in 2050 [2]. Elevated CO2 (eCO2) may enhance plant photosynthesis and biomass production [3,4,5], and consequently, increase C input to soil by stimulating fine root turnover and rhizodeposition [6,7,8], which provide important available substrates for soil microbes. Therefore, eCO2 may cause changes in soil C turnover, N availability and N2O emissions associated with microbial processes [9,10]. N2O emissions from croplands with N fertilization was responsible for 70% of global annual N2O emissions [11,12]. As N2O is a powerful greenhouse gas with 298-fold greater global warming potential than CO2 [2] and is also involved in the destruction of stratospheric ozone [13], numerous previous research focused on measuring N2O emissions under different N application rates [14,15,16]. The effect of eCO2 on N2O emissions is receiving more attention, since it can address our current knowledge gap about soil feedback of global warming. However, no consensus has been reached so far. The response of N2O emissions to eCO2 has varied in different studies, where the duration of the CO2 enrichment experiment and aboveground vegetation types were different [16,17,18].
A previous meta-analysis showed eCO2 significantly increased N2O emission by 19% in the upland soils [19]. This conclusion was further supported by a recent meta-analysis, showing the N2O emission under eCO2 increased 23% on average from various land types [20]. In addition, cropland was the only land type where a significantly positive relation was found between N2O emissions and eCO2 [20]. The effect of eCO2 in combination with N fertilization, a common agricultural management measure in cropland, can enhance the emissions of N2O [21]. In line with this viewpoint, our previous work conducted in a winter-wheat field also found that higher N application rate promoted N2O emission greater than lower N application rate under the same eCO2 level after 1.5 years of eCO2 duration [17]. It has been argued N2O emission may adapt to long-term CO2 enrichment. For example, a study based on the free air CO2 enrichment (FACE) conducted in a semi-arid grassland found no effect of eCO2 on N2O emissions after 4 years of continuous operation [22]. However, another FACE study carried out in a temperate grassland has proved a more than two-fold increase of N2O emissions after 15 years of continuous CO2 enrichment [18]. Soil nutrient availability may play a critical role in controlling the response of N2O emission to eCO2, irrespective of running time duration. As reported by the meta-analysis based on different land-use types, eCO2 exerted a significant effect on soil N2O fluxes only in N fertilized soils [5]. Although Liu et al. [5] considered that improving N availability mainly accounted for the enhanced N2O emission, the corresponding effect between N-limited natural ecosystems and N-rich agroecosystems was not distinguished. A recent report from a paddy rice field found that after 6 years of continuous observation eCO2, N2O emissions decreased obviously at an N application rate ≥ 150 kg N ha−1, but remained unaffected at an N application rate ≤ 125 kg N ha−1 [16]. It should be noted that the paddy rice fields are periodically flooded, which does not occur in cropped upland; thus, it is uncertain whether the conclusions drawn from paddy rice fields are applicable to upland farming. Due to a lack of an appropriate research platform as well as the expensive maintenance cost of the FACE facility, an associated study on upland farming is still urgently needed to expand our knowledge of how soil N2O emission responds to the long-term CO2 enrichment under different hydrothermal and N conditions.
The main N2O production processes are closely associated with soil labile C substrate and mineral N availability, as well as soil aeration and moisture [9]. Soil labile organic C comprises multiple labile organic C components, such as dissolved organic C (DOC), microbial biomass C (MBC), particulate organic C and easily oxidizable C expressed in terms of different assaying methods [23]. DOC is regarded as the most unstable component of soil labile C [24,25]. It increases greatly with added C inputs, and has a good positive linear relationship with other soil labile C components [26]. MBC represents the biologically living fraction of labile C and utilizes DOC as the main C source [27]. The two indicators were recognized as sensitive indicators to reflect eCO2-induced changes in soil labile organic C pool [28]. Liu et al. [5] reported that the positive response to eCO2 was significant for MBC (14.0%) but insignificant for DOC (6.1%), particularly in fertilized upland soils. Under eCO2, increased soil moisture may occur due to reduced stomatal conductance and increased water use efficiency of plants [29,30]. It has been reported that eCO2 increased soil CO2 emissions and, thus, may cause anoxia [31], which was associated with the greater input of root exudates to soil and enhanced soil microbial activity under eCO2 [8,10]. In addition, a number of studies have reported a significant positive linear correlation between CO2 and N2O emissions in agricultural soils [32,33]. Such increases in labile C supply, soil moisture, and lower aeration can cause higher N2O emission through enhanced denitrification, especially when soil nitrate N was high [18,19]. On the other hand, eCO2 may promote plant N uptake or microbial N immobilization, which would in turn decrease soil N availability and, thus, N2O emissions [8,16,34]. The decomposition and mineralization of organic components are mediated by soil enzyme activities, which are highly sensitive to associated substrates and could reflect both the changes in concentrations and components of soil labile C and N [35]. Responses of enzymatic activities to eCO2 have also been reported due to interferences with other factors, such as plant types, soil nutrients availability, etc. [36,37]. Soil extracellular enzymatic activities tended to be enhanced under eCO2 due to greater rhizodeposition [38,39,40]. It has been reported that the microbial biomass and activity in rhizosphere were greater than that of the bulk soil [41,42]. In addition, eCO2 could potentially change the rhizosphere environment and, thus, the microbial activities, which may further alter soil C and N turnover [43]. Therefore, investigations on soil C and N availability in both the rhizospheric and bulk soils under eCO2 are necessary in order to understand the specific fluctuation of N2O emissions under eCO2.
The winter wheat–summer maize rotation is a conventional upland cropping pattern in the North China Plain. Although both winter wheat and summer maize require large amounts of N application, the major factors affecting N2O emissions are varied, such as soil temperature, water regime, aeration condition, etc. [9]. It is important to study the response of soil N2O emissions to eCO2 in different crop seasons in intensively fertilized cropland. The N2O emission factors from summer maize fields seem higher than that from winter wheat fields due to appropriate hydrothermal conditions in the maize season [44,45]. Therefore, the present study was conducted in a summer maize field in the North China Plain based on a FACE platform, which had continuously run for 12 years at the time of this study. The key objective of this study was to investigate the effects of eCO2 on soil N2O emissions at both zero and conventional N application rates. Moreover, we also examined the dynamics of soil labile organic C components (i.e., DOC and MBC) and mineral N concentrations as well as the activities of some important extracellular enzymes in both rhizospheric and bulk soils at major growth stages during the summer maize growth period. We hypothesized that eCO2 would increase soil labile C concentrations, which could be reflected by CO2 emissions and activities of soil extracellular enzymes particularly in rhizospheric soils, and thus, cause an increase in N2O emissions adjusted by soil hydrothermal regimes, especially when combined with N fertilization.

2. Materials and Methods

2.1. Study Site

The experiment was conducted at the Chinese Academy of Agricultural Sciences Experimental Station, which was founded in 1983. This study site is located at the Changping district (40°13′ N, 116°14′ E, 72 m elevation), Beijing, in the North China Plain. It has a warm temperate continental monsoon climate with long-term (1981–2015) annual average precipitation of 600 mm (60% falling in June to August) and average air temperature of 14 °C. The cropping pattern at this study site was double cropping per year (winter wheat-summer maize/summer soybean) standing for the local cropping system. Since 2017, the planting pattern was winter wheat–summer maize. During the summer maize growing season in the year 2019, the daily mean air temperature ranged from 17.9 to 31.8 °C with an average value of 26.1 °C, and total precipitation amounted to 255.1 mm (Figure 1). The studied soil was classified as Cambisols in the semi-alfisol order of FAO soil taxonomy system with a clay loam texture [46]. Soil properties at the depth of 0–20 cm before sowing summer maize in 2019 were as follows: soil pH (H2O), 8.4; bulk density, 1.3 g cm−3; soil organic C, 12.0 g kg−1; total N, 1.6 g kg−1; alkali-hydrolyzed N, 111.8 mg kg−1; Olsen-P, 39.4 mg kg−1; available K, 157.1 mg kg−1; soil NO3--N in 0–100 cm depth, 149.4 mg kg−1.

2.2. The Experimental Design and Field Management

The experiment was carried out based on a FACE platform initiated in October 2007 and has continuously lasted for 12 years. A completely randomized design was used in the experiment with four treatments: aCO2-ZN (ambient CO2 under zero N fertilization), aCO2-CN (ambient CO2 under conventional N fertilization), eCO2-ZN (eCO2 under zero N fertilization), and eCO2-CN (eCO2 under conventional N fertilization). Three replicates were set for each treatment (in a total of 12 plots). In CN plots, granular urea was used at a rate of 180 kg N ha−1. Specifically, 40% of total N was incorporated into the soils as basal fertilization one day prior to sowing, and another 60% of total N was applied as top-dressing at the 10-extended-leaf stage by spreading followed by 50 mm sprinkling irrigation. All plots received 150 kg P2O5 ha−1 as superphosphate and 90 kg K2O ha−1 as potassium chlorate the day before sowing. In this study, Zhengdan 958, a local cultivar, was sown on 19 June 2019 and harvested on 28 September 2019, with 60 cm row spacing and 25 cm plant spacing (i.e., 6 plants in 1 m2). Irrigation was applied twice during the whole growing season with the first one applied following sowing (60 mm) and the second one (50 mm) occurred at the 10-extended-leaf stage after topdressing.
The FACE field consists of twelve octagonal rings with a diameter of 4 m, with six rings under ambient atmospheric CO2 concentrations (aCO2) and the other six rings under elevated atmospheric CO2 concentrations (eCO2) at the target CO2 concentration of 550 ppm. Rings are separated by at least 14 m to minimize CO2 contamination. The elevated and ambient atmospheric CO2 concentrations (eCO2 and aCO2) were measured throughout the growing season by sensors (Viasala, Finland) in the center of each octagonal ring about 15 cm above the canopy. In the six elevated rings, pure CO2 gas was released from octagonal emission tubes set at 15 cm above the crop canopy during daylight. The CO2 release was controlled by a computer program with an algorithm based on wind speed and direction to maintain the target CO2 concentration in the elevated CO2 rings. During the summer maize growth period, the average CO2 concentration was 567 ppm for eCO2 and 422 ppm for aCO2. The error of measured data in eCO2 during the summer maize growth period was controlled for within 20 ppm on more than 85% of days. The detailed description of this FACE experiment has been reported by Diao et al. [47] and Han et al. [48].

2.3. Gas Sampling and Assay

In situ sampling of gases was performed in the summer maize season of 2019, using the static closed chamber method [49]. The static chamber consisted of two parts, a base box and a chamber box with sizes of 50 × 25 × 20 cm and 50 × 25 × 35 cm (length × width × height), respectively. The base box was inserted 5 cm into the soil between maize rows after maize sowing and remained in situ throughout the experimental period. The gas samples were collected daily for seven days following fertilization and for three days after each rainfall (>10 mm) or single irrigation. In the other growth period, gas samples were collected once a week. Gas samples were collected between 09:00 and 10:00 in the morning on each sampling day, which could stand for the daily mean emission flux. At each sampling, 30 mL gas sample was collected at 0, 10 and 20 min after the chamber was closed and injected into a 12 mL pre-evacuated vial separately. The gas concentration increased linearly within 20 min [15]. At the same time, the air temperature in the chamber, as well as soil temperature and the volumetric water content (VWC) at the 5 cm depth, were also measured. The soil water-filled pore space (WFPS) was calculated according to Song et al. [50].
The concentrations of N2O and CO2 were analyzed within three days using a gas chromatograph (Agilent 7890B, Agilent Technologies Inc., CA, USA) equipped with electron capture detector (ECD) and a flame ionization detector (FID), with the lowest detection limits for N2O and CO2 concentrations at 32 ppb and 4 ppm, respectively. To avoid cross-interference of N2O and CO2 in the N2O analysis, we used N2 as the carrier gas with 10% CO2 as the make-up gas for measuring N2O in the ECD [51]. Standard gas mixture (315 ppb N2O and 455 ppm CO2, 439 ppb N2O and 650 ppm CO2) was analyzed after every 12 gas samples to calculate the concentrations of samples. The N2O or CO2 fluxes were calculated by linear regression, as described by Huang et al. [14]. Additionally, the cumulative N2O or CO2 emission for each treatment over the season was calculated by the cumulated emissions of each measured period. Detailed calculation methods for N2O and CO2 are described in Huang et al. [14].

2.4. Soil Sampling and Assay

Soil samples (rhizospheric and bulk soils) were collected at major growth stages, i.e., bellmouth, tasseling and maturity stage. Bulk soil (0–20 cm) was collected using a soil auger for the sparse rows. The soil tightly adhering to roots was collected by shaking the whole roots gently and defined as rhizospheric soil. All soil samples were passed through a 2-mm mesh to remove stones, crop residues and roots, and subsequently stored at 4 °C for further analysis within 7 days.
The concentration of DOC, referred to as water-extractable DOC in the present study, was measured by extracting the soil with deionized water (1:5, w/v) [52], and then assayed using a liquid TOC auto-analyzer (Elementar Inc., Hanau, Germany) after filtering through a 0.45 µm membrane. MBC concentration was determined by subtracting the K2SO4-extracted C concentration in unfumigated soil samples from that of chloroform-fumigated soil samples, divided by an extraction efficiency factor of 0.45 [53]. The concentrations of soil ammonium N (NH4+-N) and nitrate N (NO3−-N) were determined by extracting the soil with 2 M KCl solution (1:5, w/v) [18] and then analyzed with an AA3 continuous-flow analyzer (Bran + Luebbe Gmbh, Norderstedt, Germany) after filtering.
We assayed seven soil extracellular enzymes according to their use of either low- or high-molecular weight substrates and their significance in C and N cycling, including β-glucosidase (BG), β-cellobiosidase (CB) and β-xylosidase (XYL), N-acetyl-glucosaminidase (NAG) and L-leucine aminopeptidase (LAP), as well as phenol oxidase (PPO) and peroxidase (PER). The activities of BG, CB, XYL, NAG and LAP were measured using the modified fluorometric technique [54,55]. The activities of PPO and PER were measured by the modified spectrophotometrically method [56,57]. Enzyme activity was expressed as µmol g−1 h−1 dry soil.

2.5. Statistical Analyses

The statistical analyses were performed using SPSS 20.0 (IBM Corp., Armonk, NY, USA). The significance among treatments were performed using ANOVA based on the Least Significant Difference (LSD) test at a 5% probability level as the judgement standard (p < 0.05). Figures were plotted using Origin 2021 (OriginLab Corporation, Northampton, MA, USA). Data were reported as means with standard errors of three repetitions.

3. Results

3.1. Soil N2O and CO2 Emission Fluxes during the Summer Maize Growth Period

Soil N2O emission fluxes varied in the range of 10.4–634.7 μg N m−2 h−1 (Figure 2a). The N2O emission variation was characterized by two distinct high peaks and a few small pulse emissions after two N applications. The biggest N2O emission was peaked at 634.7 ± 74.9 μg N m−2 h−1 and occurred after N top-dressing, which was 1.7 times higher than the first peak valued at 371.0 ± 50.6 μg N m−2 h−1 after basal fertilization. Other small pulse peaks of N2O fluxes were presented after precipitation or irrigation, with the biggest peak value at 225.7 ± 18.4 μg N m−2 h−1, much lower than those after fertilization. For the emission peaks associated with fertilization, it usually occurred 3 days after N application and the peak lasted 4–5 days. The seasonal characteristics of N2O dynamics were similar for various treatments. However, the magnitude of N2O emissions was affected by different treatments. For the top-dressing emission peak, it was higher by 23.1% and 25.4% under eCO2 than aCO2 at zero N fertilization (ZN) and conventional N fertilization (CN) levels, respectively. For the emission peak after basal fertilization, it was 11.6% and 25.4% higher under eCO2 than aCO2 at ZN and CN levels, respectively. It was also 9.4–39.6% higher under eCO2 than aCO2 at other small emission peaks after precipitation and irrigation events.
Soil CO2 fluxes were fluctuated between 131.2 ± 13.9 and 316.9 ± 36.6 mg C m−2 h−1 within two weeks after basal fertilization event (Figure 2b). After basal fertilization, there were a few pulse peaks with the highest peak of 261.2 ± 16.6 mg C m−2 h−1 occurring after N top-dressing and rainfall events. Soil CO2 fluxes decreased consistently in all treatments since mid-August, in accordance with the dropping of soil temperature (Figure 2c). The increase of soil CO2 fluxes under eCO2 was in line with the observation in soil N2O fluxes. The seasonal average of CO2 emission flux under eCO2 was 9.2% and 14.1% higher than aCO2 for ZN and CN levels, respectively.
The cumulative N2O emissions ranged from 1.66 to 2.55 kg N ha−1, and it was increased by 12.4% (p = 0.064) and 15.6% (p = 0.057) for ZN and CN levels, respectively, under eCO2 compared to those under aCO2 (Table 1). N fertilization significantly increased cumulative N2O emissions by 33.1% under aCO2 and 36.9% under eCO2. In addition, N fertilization under aCO2 generated obvious greater cumulative N2O emissions than no N fertilization under eCO2. The direct N2O emission factor was 0.31% under aCO2, which was not distinguished from the 0.39% under eCO2, but both were lower than the default value of 1.1% in the IPCC guideline [58]. The cumulative CO2 emissions varied between 3010.4–4175.2 kg C ha−1, and significant increases were observed under eCO2 by 13.8% and 18.5% at ZN and CN levels, respectively, compared with those under aCO2 (Table 1). N fertilization significantly increased cumulative soil CO2 emissions by 17.0% and 21.8% under aCO2 and eCO2, respectively. However, there was no difference between the cumulative soil CO2 emissions from ZN under eCO2 and CN under eCO2.

3.2. Soil DOC and MBC Concentrations at Major Stages during the Summer Maize Growth Period

Figure 3a shows the variation of soil DOC concentration at three major growth stages including bellmouth, tasseling and maturity at both the rhizospheric and bulk soils in different treatments. Overall, the averaged DOC showed the highest value of 83.4 ± 0.8 mg kg−1 at the bellmouth stage and dropped to the lowest value of 44.9 ± 1.0 mg kg−1 at the maturity stage. DOC in the rhizospheric soils were higher by 7.0–25.8% than in the bulk soils in different treatments. It was increased by 5.6–12.1% and 1.6–8.3% at the rhizospheric and bulk soils under eCO2 compared to aCO2, respectively. The increase of DOC under eCO2 was consistent and significant across tasseling and maturity stages, in both rhizospheric and bulk soils.
The monitored MBC concentration ranged from 290.0 ± 1.0 mg kg−1 to 470.4 ± 2.9 mg kg−1 across the three growth stages and it was 4.3–33.2% higher in rhizospheric soils than in bulk soils (Figure 3b). eCO2 exhibited increases in MBC by 2.6–16.8% in rhizospheric soils compared to aCO2, showing a significant increase ever since tasseling stage. MBC in the bulk soils under eCO2 was also increased by 1.4–6.8% compared to aCO2, but did not reach statistical significance at the three stages. N fertilization obviously increased MBC at both rhizospheric and bulk soils across the latter two growth stages, which was unaffected by CO2 treatment.

3.3. Soil Mineral N Concentration at Major Stages during the Summer Maize Growth Period

Soil mineral N concentration and pH were also measured at three major stages (i.e., bellmouth, tasseling and maturity) during the maize growth period (Figure 4). For soil NH4+-N (Figure 4a), its concentration ranged about 7.4–10.0 mg kg−1 for different treatments at the bellmouth stage and then decreased to 3.0–5.8 mg kg−1 until the maturity stage, perhaps due to strong mineralization and nitrification under appropriate hydrothermal conditions (Figure 2c) combined with vigorous growing requirement by plants at the bellmouth stage. The sampling date for soils at the bellmouth stage was on the fifth day after urea topdressing; therefore, the NH4+-N was higher at this stage for the fertilized plots. There was no obvious difference for the NH4+-N between the rhizospheric and bulk soils. Both CO2 concentration and N fertilization significantly influenced soil NH4+-N at the major stages; for instance, fertilized plots had higher NH4+-N concentration in the bulk soil at the bellmouth stage, as well as in the rhizospheric soil at the tasseling stage. Under the eCO2 condition, concentrations of NH4+-N were significantly lower compared to the aCO2 condition in the unfertilized plots at the bellmouth stage and tasseling stage (only in rhizospheric soils), implying that the rhizospheric zone had less NH4+-N due to possible microcosm conditions. The significant interaction of CO2 concentration and N fertilization on NH4+-N was only observed in the rhizospheric zone at the tasseling stage.
The soil NO3−-N in CN plots was around 2.8–10.5 mg kg−1 in the rhizospheric soils and 7.5–28.4 mg kg−1 in the bulk soils at the three major stages with the order bellmouth > tasseling > maturity (Figure 4b). The concentration of soil NO3−-N in the rhizospheric soil was lower by 7.8–49.5% than that in the bulk soil. Soil NO3−-N was affected remarkably by the CO2 concentration, except for that in the rhizospheric soils at the maturity stage. For soil NO3−-N in ZN plots, it varied in the range of 2.7–6.2 mg kg−1 and there was no significant difference between rhizospheric and bulk soils. Similar to soil NH4+-N, the concentration of soil NO3−-N was also reduced under eCO2 in the range of 15.0–35.2% and 4.2–30.5% in ZN and CN plots, respectively, showing significance in the bulk soils.

3.4. Soil Extracellular Enzymatic Activities at Major Stages during the Summer Maize Growth Period

We measured the activities of seven soil extracellular enzymes, including three carbohydrate-related enzymes (CRE) and two amino-group transfer related enzymes (ATE), as well as two oxidases at the three stages, as shown in Figure 5.
For the CRE enzymes (Figure 5a–c), their activities were 73.9–130.6 µmol g−1 h−1, 11.7–36.7 µmol g−1 h−1 and 33.2–100.0 µmol g−1 h−1 for BG, CB and XYL, respectively. Across the three growth stages, eCO2 promoted the activities of three CREs, to a greater or lesser degree, both in CN and ZN plots in comparison to aCO2 at most of the stages, particularly at the bellmouth and tasseling stages. N fertilization significantly promoted the activities of CREs at both bellmouth and tasseling stages in rhizospheric soils. Although the interaction between eCO2 and N fertilization on CREs was almost not significant, their combined effect (aCO2-ZN vs. eCO2-CN) significantly increased CREs, such as BG and XYL in rhizospheric soils. The activities of ATE (Figure 5d,e) fluctuated around 4.23–8.16 µmol g−1 h−1 and 122.7–209.5 µmol g−1 h−1 for NAG and LAP, respectively. NAG exhibited a significant increase under eCO2 at the bellmouth stage. N fertilization did not increase and even reduced NAG activity significantly at the bellmouth stage, while N fertilization significantly increased LAP activity at the maturity stage in rhizospheric soils. The interaction between eCO2 and N fertilization on ATEs was not significant.
For oxidases activities (Figure 5f,g), their activities were very close in the value, ranging about 0.68–1.73 µmol g−1 h−1 and 0.52–1.71 µmol g−1 h−1 for PER and PPO, respectively. PER showed significant increases under eCO2 at the tasseling stage, while PPO exhibited significant increases under eCO2 at the bellmouth stage in rhizospheric soils. N fertilization significantly increased oxidases activities, and the interaction between eCO2 and N fertilization on oxidases activities was significant for PER at the maturity stage.

3.5. Correlation Coefficients and Regression Analyses between N2O Emissions and Soil Parameters

The N2O emission could reflect the intensity of nitrification and denitrification and their hydrothermal regimes, while soil CO2 emissions may usually reflect the status of soil respiration derived from labile C to a certain extent. There were important interlinkages between N2O flux and other soil parameters (Table 2). In general, significant and positive correlations were found between N2O flux and associated parameters, such as soil CO2 flux, soil temperature and WFPS. Soil N2O flux was positively correlated with DOC and NH4+-N concentration significantly, and negatively correlated with the activities of XYL and LAP significantly, in both rhizospheric and bulk soils. Moreover, the rhizospheric soil displayed higher coefficients with DOC, NH4+-N concentration and XYL activity, but lower coefficients with LAP activity. In addition, soil N2O flux showed a significant negative correlation with MBC concentration and positive correlation with NAG activity in the rhizospheric soil. Additionally, N2O flux reflected a significant negative correlation with BG activity in the bulk soil.
According to the stepwise regression analysis, the major controlling factors for N2O flux mainly included soil CO2 flux, NO3−-N and NH4+-N concentration in this study.

4. Discussion

4.1. The Response of N2O Emissions to eCO2

Our results showed that the seasonal N2O emissions (ranging from 1.66 to 2.55 kg N ha−1) were increased by eCO2 in both ZN and CN plots at marginal significance levels (12.4% (p = 0.064) and 15.6% (p = 0.057), respectively; Figure 2a, Table 1). Our experiment showed less increases of N2O emissions under eCO2 compared with a recent meta-analysis result of Wang et al. [20], which showed that eCO2 caused on average a significant increase in N2O emissions from croplands by 38%. However, our previous results have shown that eCO2 increased seasonal N2O emissions greatly, by as much as 51.5–65.9% at the same summer-maize field in the year 2017 and 2018 [59]. The varied increase extent of N2O emissions to eCO2 in different years usually could be associated with soil hydrothermal regimes, which have a major effect on soil N2O fluxes [60]. The rainfall in the summer maize growth period in this study (255.1 mm in 2019) was significantly lower than in the previous two years (442.6 mm in 2017 and 349.6 mm in 2018 [59]), while the mean air temperatures in the summer maize growth period were comparable across the three study years (around 26 °C). With high evaporation and transpiration rates during summer, our supplementary light irrigation in June and August and light rainfall resulted in lower soil moisture after fertilization (33.7–49.8% WFPS) in the study year (Figure 2c) compared to that in the previous two years (50.0–62.8% WFPS) [59]. Another study conducted in the N-fertilized calcareous fluvo-aquic soils in the summer maize season in the warm temperate zone also suggested that N2O emissions were greatly related with the WFPS [61]. Our results, in line with the work of [61], implied that the soil water regime could affect the response of N2O emissions to eCO2. Therefore, we support the view that eCO2 exerts a positive effect on N2O emissions, although it varied under different hydrothermal conditions in the cropland soil, just as the great majority of papers have indicated [19,20,62,63].
Nitrification and denitrification are the main processes involved in soil N2O production [9]. In our previous study, under eCO2, soil potential nitrification rate (PNR) and potential denitrification rate (PDR) showed a significant increase of 36.4% and 59.0%, respectively [59]. However, different hydrothermal regimes could affect the intensities of N transformation processes and, thus, influence N2O emission. At a soil water content range of around 35–60% WFPS, the contribution of nitrification to N2O emissions was increased with the increase of soil WFPS [64]. Moreover, in the fertilized upland soil, nitrifier denitrification was reported to be the main pathway of N2O emissions due to sub-aeration after a few days after fertilization combined with irrigation, which derived from oxygen depletion by strong ammonia oxidization following ammonium-N application, the first step of the nitrification process [65,66,67]. It was reported that nitrifier denitrification contributed about 60% of the total N2O emissions during the earlier period of N application in the typical calcareous soil [65]. Zhu et al. [67] found that the total N2O emissions decreased 19-fold when the O2 concentration increased from 3% to 21%, and the contribution of nitrifier denitrification reduced from 57% to 38% on average in urea-amended soil. In N-rich alkaline soils, the nitrifier denitrification process is performed by ammonia-oxidizing bacteria (AOB) [65,68]. It is notable that genes encoding N2O reductase have not been found in AOB genomes [69], and therefore, nitrifier denitrification might be a net N2O production process. Plant root exudates addition has been reported to increase the contribution of nitrifier denitrification and denitrification to soil N2O emission [70]. However, the soil moisture in the experimental year was lower than 50.0% WFPS after fertilization (Figure 2c), which could result in good aeration and weak denitrification and nitrification, particularly the associated lower nitrifier denitrification. Consequently, possible N2O emissions from both nitrification and denitrification occurred under higher aeration, coinciding with lower moisture, were exhibited in the experimental year in this study. Under this condition (lower WFPS and higher aeration), the response of N2O emissions to eCO2 could be weak, similar to the observed marginally significant increase of 12.4–15.6% in this study, and lower than the results under the appropriate soil moisture regime of 30–60% WFPS, which is the preferred aeration range for nitrifier denitrification after fertilization in the cropland soil. This was in line with the results at the Giessen FACE field site, where the eCO2 effect was non-detectable in low soil moisture block, but increased at the blocks with intermediate to high soil moisture [62,71]. Moreover, a significant response of soil N2O emissions (2.88-fold) to 15-year eCO2 duration was observed under soil WFPS, ranging from 40–112% (conversion from soil volumetric water contents of 25–70%) in Giessen FACE [18].
Through the comprehensive analyses on the possible conditions of N2O processes under eCO2, we draw the frame pathways on N2O emissions under eCO2, as shown in Figure 6. Generally, eCO2 increased available C inputs in the soil by C-deposition, thereby increasing soil labile C (i.e., DOC and MBC). This can stimulate microbial growth and soil extracellular enzyme activities (CRE) for catalyzing the decomposition of compounds such as DOC and so on, which accelerated the soil microbial respiration and, thus, soil CO2 emission. In turn, this might lead to sub-aerobic microsites favoring denitrification and nitrifier denitrification to produce more N2O. However, contrast analyses also found that instant environmental factors after fertilization, such as soil moisture, could influence the inter-annual variations and response of N2O emissions to eCO2. Hence, long-term continuous monitoring on N2O emissions under various hydrothermal regimes are greatly required based on the FACE platform, in order to understand the comprehensive role of eCO2 on N2O emissions under future climate change, with eCO2, rising temperature and staged drought as major properties. We also propose that a meta-analysis needs to classify the major influencing factors, including the soil hydrothermal index, in order to reveal the comprehensive characteristics of eCO2 on N2O emissions.

4.2. Changes of Soil Labial Organic C Components and Mineral N under eCO2

Besides actual environmental conditions (e.g., soil moisture), it is well recognized that soil N2O emissions are regulated by C availability [9], especially soil labile C component [19], since it generally stimulated denitrification [72]. Additionally, increased C availability also enhances microbial activity and, consequently, in situ O2 consumption, which may lead to the sub-aerobic microsites facilitating N2O emission by denitrification and nitrifier denitrification [8,50].
Our measurement showed that eCO2 significantly increased the concentrations of DOC and MBC, two sensitive indicator of soil labile C component [28], by 1.6–12.1% and 1.4–16.8%, respectively, in the rhizospheric soils at both tasseling and maturity stages (Figure 3). This was consistent with a summary based on 68 studies, which showed that eCO2 increased DOC and MBC by 6.1% and 14.0%, respectively, in the fertilized upland soil [5]. This could be explained by some studies [10,73], which reported that eCO2 tended to enhance below-ground C allocation, including root exudation and root biomass, which stimulated microbial activities (e.g., the increases in BG activity (Figure 5a)) and soil organic matter decomposition due to priming effects. Hu et al. [74] also reported that eCO2 significantly increased the DOC content by 23% and increased the MBC content by 15%. In our study, the presence of soil labile C components in CN plots was significantly higher than that in ZN plots (Figure 3), which might be due to the enhancement in rhizodeposition and microbial growth under N fertilization [8,75]. In addition, soil cumulative CO2 emissions were significantly increased by 13.8–18.5% under eCO2 compared to aCO2 (Figure 2b, Table 1), which implied that the decomposition of increased DOC and other components may be promoted. Our previous study also observed an increase of MBC by 2.1-fold under eCO2 in the maize season in 2018 [47]. In this study, the increasing percentage of labile organic C components under eCO2 was relatively lower than other studies [74,76], which could be linked to lower soil moisture regimes. It has been reported that higher DOC and MBC contents occurred at greater soil moisture [77,78], while in the present study, soil moisture was low, and most of the time, soil WFPS was below 40% (Figure 2c). Moreover, low soil moisture could also reduce the diffusion of substrates to microbes and weaken microbial activity [79], despite the additional supply of labile C-substrate under eCO2. This is partly supported by the less increases in enzymatic activities under eCO2 (Figure 5).
In contrast to the labile C components, soil mineral N contents showed a negative response to eCO2 irrespective of the N application rate (Figure 4). In other studies, eCO2 also seemed to reduce soil mineral N [80,81,82,83]. This was probably due to more N demand by plants and microbes as a result of higher photosynthetic C accumulation in biomass and more C entering soil under eCO2 [83,84]. Our other study conducted in the same field has showed that the total N uptake in above-ground biomass of maize was slightly increased under eCO2 [85]. In addition, the stimulation of N immobilization by higher microbial activities under eCO2 may also partly account for the decline in NH4+-N and NO3−-N concentrations based on the necessary C:N ratio at increased MBC under eCO2 [86].

4.3. Changes of Soil Extracellular Enzyme Activities under eCO2

The activities of soil enzymes targeting specific compounds or nutrient acquisitions could reflect the status of associated substrates [35]. Similar to labile organic C components, the activities of CRE were increased under eCO2, particularly in rhizospheric soils at the tasseling stages (Figure 5a–c). This indicated that eCO2 could stimulate soil microbial activities and the associated CO2 efflux from soil (Figure 2b). Under eCO2, the increases in CRE activities seem to be a stimulative reflect of increased C input derived from root exudation and other dead organic debris [39,40,73]. As reviewed by [87], eCO2 increased the efflux amount of C-rich root exudates by 31%, which was likely ascribed to increased root biomass, as well as the efflux rates of some specific compounds, including total carboxylates by 111% and total soluble sugars by 47%. Most CREs and some ATEs exhibited higher activities at most stages particularly at the tasseling stage in this study (Figure 4a–c,e), consistent with other studies [40,88,89]. The combination of eCO2 and N fertilization significantly increased three CREs at some stages (Figure 5a–c). It contrasted with the study of Zhao et al. [90] in an alpine meadow on the Tibetan Plateau, which reported decreased CREs (e.g., CB, BG and XYL) when eCO2 was coupled with N fertilization. This positive response suggests that N supply appears to promote soil microbes to produce more C-related enzymes due to more nutrient supply to microbes at low energy acquisition costs [91].
The activities of ATEs under eCO2 exhibited an increase for LAP and decrease for NAG only at the bellmouth stage, and N fertilization did not increase and even reduced ATEs activities, despite being under eCO2, except at the maturity stage of rhizospheric soils (Figure 5d,e). Our results were similar to previous studies, which might be interpreted by the fact that microbial activity did not appear to be limited by N in our study [88,92]. Furthermore, the increased C allocation to roots under eCO2 induced the nutrients demand of plants and microorganisms, and the N application timely met the nutrient requirement by microbes [86,93]. N fertilization also increased oxidases activities (i.e., PPO and PER), particularly under eCO2 (Figure 5f,g), implying that N supply may promote the degradation of complex compounds (e.g., phenolics and lignin) and recalcitrant soil organic matter under eCO2 [94,95].
However, in this study, the responses of enzymatic activities to eCO2 were not strong under lower WFPS, compared to previous studies with higher enzymatic activities under appropriate soil moisture [92,96]. At low soil moisture, diffusion of soluble substrates and enzyme mobility become limited [97]. On the other hand, in the soils subjected to low soil moisture, microbes shift resource allocation to relieve the drought physiological stress, potentially slowing down the flows of C and N and, thus, downregulating the production of extracellular enzymes [98].

5. Conclusions

Based on the long-term FACE platform in the North China Plain, our study shows that 12 years of CO2 enrichment increased soil N2O emissions in a maize field, and eCO2 combined with N fertilization increased the intensity of soil N2O emissions. However, lower soil moisture may have caused the lower response of N2O emissions to eCO2. eCO2 significantly increased soil CO2 emissions, as well as the activities of soil extracellular enzymes at the major maize growth stages, which occurred concurrently with the associated increase of DOC and MBC concentrations in the soils under eCO2. In contrast, soil mineral N contents were decreased under eCO2, likely due to more N demand by plants and microbes under eCO2. Overall, our results highlight that environmental factors such as soil moisture influence the response extent of N2O emissions to eCO2. Hence, continuous monitoring of N2O emissions and analyses of N2O production pathways under various hydrothermal regimes are further required based on FACE platform in intensively fertilized cropland soils.

Author Contributions

Conceptualization, F.M. and L.G.; methodology, L.G.; software, X.H. and K.L.; validation, F.M., M.L. and N.W.; formal analysis, F.M. and L.G.; investigation, F.M. and L.D.; resources, L.G.; data curation, F.M., M.L. and L.D.; writing—original draft preparation, F.M.; writing—review and editing, F.M., L.G. and X.Z.; visualization, F.M.; supervision, L.G.; project administration, L.G. and X.Z.; funding acquisition, L.G. and X.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (31901174) and the National Key R&D Program of China (2017YFD0300301). The Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences also supported this study.

Data Availability Statement

The data supporting the conclusions of this article are included within the paper.

Acknowledgments

We thank Niu Xiaoguang, Zhu Guohong and Xu Yong for their help in managing the maize field.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Variations of air temperature and daily precipitation during the summer maize growth season.
Figure 1. Variations of air temperature and daily precipitation during the summer maize growth season.
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Figure 2. Dynamics of soil N2O (a) and CO2 (b) fluxes and associated variation of soil temperature and moisture (water-filled pore space, WFPS) (c) during the summer maize growth period. aCO2, eCO2, ZN and CN refer to ambient CO2, elevated CO2, zero N fertilization and conventional N fertilization, respectively.
Figure 2. Dynamics of soil N2O (a) and CO2 (b) fluxes and associated variation of soil temperature and moisture (water-filled pore space, WFPS) (c) during the summer maize growth period. aCO2, eCO2, ZN and CN refer to ambient CO2, elevated CO2, zero N fertilization and conventional N fertilization, respectively.
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Figure 3. The dynamics of DOC and MBC concentrations at major stages during the summer maize growth period. Different letters indicate a significant difference (p < 0.05) between treatments in the same stage. Two-way ANOVA results are used to determine the significances and interactions among the effects of elevated CO2 (CO2) and N fertilization (N) on DOC and MBC concentrations (n.s., p > 0.05; *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001). aCO2, eCO2, ZN and CN refer to ambient CO2, elevated CO2, zero N fertilization and conventional N fertilization, respectively.
Figure 3. The dynamics of DOC and MBC concentrations at major stages during the summer maize growth period. Different letters indicate a significant difference (p < 0.05) between treatments in the same stage. Two-way ANOVA results are used to determine the significances and interactions among the effects of elevated CO2 (CO2) and N fertilization (N) on DOC and MBC concentrations (n.s., p > 0.05; *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001). aCO2, eCO2, ZN and CN refer to ambient CO2, elevated CO2, zero N fertilization and conventional N fertilization, respectively.
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Figure 4. The dynamics of soil NH4+-N and NO3−-N concentrations at major stages during the summer maize growth period. Different letters indicate a significant difference (p < 0.05) between treatments in the same stage. Two-way ANOVA results are used to determine the significances and interactions among the effects of elevated CO2 (CO2) and N fertilization (N) on NH4+-N and NO3−-N concentrations (n.s., p > 0.05; *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001). aCO2, eCO2, ZN and CN refer to ambient CO2, elevated CO2, zero N fertilization and conventional N fertilization, respectively.
Figure 4. The dynamics of soil NH4+-N and NO3−-N concentrations at major stages during the summer maize growth period. Different letters indicate a significant difference (p < 0.05) between treatments in the same stage. Two-way ANOVA results are used to determine the significances and interactions among the effects of elevated CO2 (CO2) and N fertilization (N) on NH4+-N and NO3−-N concentrations (n.s., p > 0.05; *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001). aCO2, eCO2, ZN and CN refer to ambient CO2, elevated CO2, zero N fertilization and conventional N fertilization, respectively.
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Figure 5. The dynamics of soil enzymatic activities at major stages during the summer maize growth period. Different letters indicate a significant difference (p < 0.05) between treatments in the same stage. Two-way ANOVA results are used to determine the significances and interactions among the effects of elevated CO2 (CO2) and N fertilization (N) on soil enzyme activities (n.s., p > 0.05; *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001). aCO2, eCO2, ZN and CN refer to ambient CO2, elevated CO2, zero N fertilization and conventional N fertilization, respectively.
Figure 5. The dynamics of soil enzymatic activities at major stages during the summer maize growth period. Different letters indicate a significant difference (p < 0.05) between treatments in the same stage. Two-way ANOVA results are used to determine the significances and interactions among the effects of elevated CO2 (CO2) and N fertilization (N) on soil enzyme activities (n.s., p > 0.05; *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001). aCO2, eCO2, ZN and CN refer to ambient CO2, elevated CO2, zero N fertilization and conventional N fertilization, respectively.
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Figure 6. A frame mechanism of N2O pathways under eCO2.
Figure 6. A frame mechanism of N2O pathways under eCO2.
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Table
Table 1. The cumulative N2O and CO2 emissions under different treatments.
Table 1. The cumulative N2O and CO2 emissions under different treatments.
TreatmentN Application Rate
(kg N ha−1)		Cumulative N2O
(kg N ha−1)		N2O Emission
Factor (%)		Cumulative CO2
(kg C ha−1)
aCO2-ZN01.66 b—3010.4 c
eCO2-ZN01.87 b—3426.7 b
aCO2-CN1802.21 a0.31 a3524.0 b
eCO2-CN1802.55 a0.39 a4175.2 a
The direct N2O emission factor was determined by subtracting the cumulative N2O emissions in CN plots from that of ZN plots, divided by the total N application rate of 180 kg N ha−1. Different letters in each column indicate a significant difference (p < 0.05) between treatments. aCO2, eCO2, ZN and CN refer to ambient CO2, elevated CO2, zero N fertilization and conventional N fertilization, respectively.
Table
Table 2. Pearson correlation coefficients and multiple stepwise regression models between N2O flux and associated soil parameters in rhizospheric soil and bulk soil, respectively (n = 36).
Table 2. Pearson correlation coefficients and multiple stepwise regression models between N2O flux and associated soil parameters in rhizospheric soil and bulk soil, respectively (n = 36).
CO2TWFPSDOCMBCNH4+-NNO3−-NBGCBXYLNAGLAPPPOPER
Rhizospheric soil 0.60 **−0.32 *0.46 **0.16−0.10−0.14−0.43 **0.35 *−0.28 *0.23−0.07
Bulk soil0.66 **0.63 **0.61 **0.45 **0.240.37 *0.07−0.54 **−0.19−0.34*−0.22−0.39 **0.160.12
Multiple stepwise regression model
Rhizospheric soilN2O = 1.241CO2 ** − 6.514NO3−-N * + 3.532
Bulk soilN2O = 0.934CO2 ** − 2.179NO3−-N * – 8.737NH4+-N * + 1.818
CO2 and T refer to soil CO2 flux and soil temperature, respectively. * and ** indicate significance at 0.05 and 0.01 level, respectively.
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Ma, F.; Li, M.; Wei, N.; Dong, L.; Zhang, X.; Han, X.; Li, K.; Guo, L. Impacts of Elevated Atmospheric CO2 and N Fertilization on N2O Emissions and Dynamics of Associated Soil Labile C Components and Mineral N in a Maize Field in the North China Plain. Agronomy 2022, 12, 432. https://doi.org/10.3390/agronomy12020432

AMA Style

Ma F, Li M, Wei N, Dong L, Zhang X, Han X, Li K, Guo L. Impacts of Elevated Atmospheric CO2 and N Fertilization on N2O Emissions and Dynamics of Associated Soil Labile C Components and Mineral N in a Maize Field in the North China Plain. Agronomy. 2022; 12(2):432. https://doi.org/10.3390/agronomy12020432

Chicago/Turabian Style

Ma, Fen, Ming Li, Na Wei, Libing Dong, Xinyue Zhang, Xue Han, Kuo Li, and Liping Guo. 2022. "Impacts of Elevated Atmospheric CO2 and N Fertilization on N2O Emissions and Dynamics of Associated Soil Labile C Components and Mineral N in a Maize Field in the North China Plain" Agronomy 12, no. 2: 432. https://doi.org/10.3390/agronomy12020432

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